Hydrogen sulfide (HS) is a respiratory toxicant that creates extreme environments tolerated by few organisms. HS is also produced endogenously by metazoans and plays a role in cell signaling. The mechanisms of HS toxicity and its physiological functions serve as a basis to discuss the multifarious strategies that allow animals to survive in HS-rich environments. Despite their toxicity, HS-rich environments also provide ecological opportunities, and complex selective regimes of covarying abiotic and biotic factors drive trait evolution in organisms inhabiting HS-rich environments. Furthermore, adaptation to HS-rich environments can drive speciation, giving rise to biodiversity hot spots with high levels of endemism in deep-sea hydrothermal vents, cold seeps, and freshwater sulfide springs. The diversity of HS-rich environments and their inhabitants provides ideal systems for comparative studies of the effects of a clear-cut source of selection across vast geographic and phylogenetic scales, ultimately informing our understanding of how environmental stressors affect ecological and evolutionary processes.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Abel DC, Koenig CC, Davis WP. 1987. Emersion in the mangrove forest fish Rivulus marmoratus: a unique response to hydrogen sulfide. Environ. Biol. Fishes 18:67–72 [Google Scholar]
  2. Affonso E, Rantin F. 2005. Respiratory responses of the air-breathing fish Hoplosternum littorale to hypoxia and hydrogen sulfide. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 141:275–80 [Google Scholar]
  3. Bagarinao T. 1992. Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquat. Toxicol. 24:21–62 [Google Scholar]
  4. Bagarinao T, Lantin-Olaguer I. 1999. The sulfide tolerance of milkfish and tilapia in relation to fish kills in farms and natural waters in the Philippines. Hydrobiologia 382:137–50 [Google Scholar]
  5. Bagarinao T, Vetter RD. 1989. Sulfide tolerance and detoxification in shallow water marine fishes. Mar. Biol. 103:291–302 [Google Scholar]
  6. Beauchamp RO, Bus JS, Popp CS, Boreiko CJ, Andjelkovich DA. 1984. A critical review of the literature on hydrogen sulfide. CRC Crit. Rev. Toxicol. 13:25–97 [Google Scholar]
  7. Beinart RA, Sanders JG, Faure B, Sylva SP, Lee RW. et al. 2012. Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses. PNAS 109:E3241–50 [Google Scholar]
  8. Belkin S, Nelson DC, Jannasch HW. 1986. Symbiotic assimilation of CO2 in the two hydrothermal vent animals, the mussel Bathymodiolus thermophilus and the tubeworm Riftia pachyptila. Biol. Bull. 170:110–21 [Google Scholar]
  9. Bernardino AF, Levin LA, Thurber AR, Smith CR. 2012. Comparative composition, diversity and trophic ecology of sediment macrofauna at vents, seeps and organic falls. PLOS ONE 7:e33515 [Google Scholar]
  10. Black MB, Lutz RA, Vrijenhoek RC. 1994. Gene flow among vestimentiferan tube worm (Riftia pachyptila) populations from hydrothermal vents of the Eastern Pacific. Mar. Biol. 120:33–39 [Google Scholar]
  11. Bolnick DI. 2004. Can intraspecific competition drive disruptive selection? An experimental test in natural populations of stickleback. Evolution 87:608–18 [Google Scholar]
  12. Brown JH, Marquet PA, Taper ML. 1993. Evolution of body size: consequences of an energetic definition of fitness. Am. Nat. 142:573–84 [Google Scholar]
  13. Bruneaux M, Mary J, Verheye M, Lecompte O, Poch O. et al. 2013. Detection and characterization of mutations responsible for allele-specific protein thermostabilities at the Mn-superoxide dismutase gene in the deep-sea hydrothermal vent polychaete Alvinella pompejana. J. Mol. Evol. 76:295–310 [Google Scholar]
  14. Budde MW, Roth MB. 2010. Hydrogen sulfide increases hypoxia-inducible factor-1 activity independently of von Hippel-Landau tumor suppressor-1 in C. elegans. Mol. Biol. Cell 21:212–17 [Google Scholar]
  15. Calvert JW, Jha S, Gundewar S, Elrod JW, Ramachandran A. et al. 2009. Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ. Res. 105:365–74 [Google Scholar]
  16. Canfield DE. 2001. Biogeochemistry of sulfur isotopes. Rev. Mineral. 43:607–36 [Google Scholar]
  17. Cary SC, Giovannoni SJ. 1993. Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. PNAS 90:5695–99 [Google Scholar]
  18. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB. 1981. Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–42 [Google Scholar]
  19. Chen K, Morris J. 1972. Kinetics of oxidation of aqueous sulfide by O2. Environ. Sci. Technol. 6:529–37 [Google Scholar]
  20. Childress JJ, Fisher CR, Favuzzi JA, Kochevar RE, Sanders NK, Alayse AM. 1991. Sulfide-driven autotrophic balance in the bacterial symbiont-containing hydrothermal vent tubeworm, Riftiapachyptila Jones. Biol. Bull. 180:135–53 [Google Scholar]
  21. Childress JJ, Girguis PR. 2011. The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities. J. Exp. Biol. 214:312–25 [Google Scholar]
  22. Comtet T, Desbruyères D. 1998. Population structure and recruitment in mytilid bivalves from the Lucky Strike and Menez Gwen hydrothermal vent fields (37°17′N and 37°50′N on the Mid-Atlantic Ridge). Mar. Ecol. Prog. Ser. 163:165–77 [Google Scholar]
  23. Cooper CE, Brown GC. 2008. The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J. Bioenerg. Biomembr. 40:533–39 [Google Scholar]
  24. Cooper D, Cooper W, de Mello W, Saltzman E, Zika R. 1989. Variability of biogenic sulfur emissions from Florida wetlands. Biogenic Sulfur in the Environment E Saltzman, W Cooper 31–43 Washington, DC: Am. Chem. Soc. [Google Scholar]
  25. Covich A. 1981. Chemical refugia from predation for thin-shelled gastropods in a sulfide-enriched stream. Verh. Int. Ver. Limnol. 21:1632–36 [Google Scholar]
  26. Cowart DA, Halanych KM, Schaeffer SW, Fisher CR. 2014. Depth-dependent gene flow in Gulf of Mexico cold seep Lamellibrachia tubeworms (Annelida, Sibolinidae). Hydrobiologia 736:139–54 [Google Scholar]
  27. De Buron I, Morand S. 2004. Deep-sea hydrothermal vent parasites: Why do we not find more. Parasitology 128:1–6 [Google Scholar]
  28. Degn H, Kristensen B. 1981. Low sensitivity of Tubifex sp. respiration to hydrogen sulfide and other inhibitors. Comp. Biochem. Physiol. B Comp. Biochem. 69:809–17 [Google Scholar]
  29. Distel DL. 2000. Phylogenetic relationships among Mytilidae (Bivalivia): 18S rRNA data suggest convergence in mytilid body plans. Mol. Phylogenet. Evol. 15:25–33 [Google Scholar]
  30. Distel DL, Baco AR, Chuang E, Morrill W, Cavanaugh C, Smith CR. 2000. Marine ecology: Do mussels take wooden steps to deep-sea vents?. Nature 403:725–26 [Google Scholar]
  31. Dubilier N, Bergin C, Lott C. 2008. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat. Rev. Microbiol. 6:725–40 [Google Scholar]
  32. Dubilier N, Giere O, Grieshaber M. 2005. Concomitant effects of sulfide and hypoxia on the aerobic metabolism of the marine oligochaete Tubificoides benedii. J. Exp. Zool. 269:287–98 [Google Scholar]
  33. Eghbal MA, Pennefather PS, O'Brien PJ. 2004. H2S cytotoxicity mechanism involves reactive oxygen species formation and mitochondrial depolarisation. Toxicology 203:69–76 [Google Scholar]
  34. Elshahed MS, Senko JM, Najar FZ, Kenton SM, Roe BA. et al. 2003. Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring. Appl. Environ. Microbiol. 69:5609–21 [Google Scholar]
  35. Faure B, Jollivet D, Tanguy A, Bonhomme F, Bierne N. 2009. Speciation in the deep sea: multi-locus analysis of divergence and gene flow between two hybridizing species of hydrothermal vent mussels. PLOS ONE 4:e6485 [Google Scholar]
  36. Garcia-Bereguiain MA, Samhan-Arias AK, Martin-Romero FJ, Gutierrez-Merino C. 2008. Hydrogen sulfide raises cytosolic calcium in neurons through activation of L-type Ca2+ channels. Antioxid. Redox Signal. 10:31–42 [Google Scholar]
  37. Gaudron SM, Marqué L, Thiébaut E, Riera P, Duperron S, Zbinden M. 2015. How are microbial and detrital sources partitioned among and within gastropod species at the East Pacific Rise hydrothermal vents. Mar. Ecol. 36:18–34 [Google Scholar]
  38. Gebruk AV, Southward EC, Kennedy H, Southward AJ. 2000. Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J. Mar. Biol. Assoc. 80:485–99 [Google Scholar]
  39. Gershoni M, Templeton A, Mishmar D. 2009. Mitochondrial bioenergetics as a major motive force of speciation. Bioessays 31:642–50 [Google Scholar]
  40. Giere O. 1993. Meiobenthology Heidelberg, Ger.: Springer [Google Scholar]
  41. Goffredi SK, Jones WJ, Erhlich H, Springer A, Vrijenhoek RC. 2008. Epibiotic bacteria associated with the recently discovered Yeti crab. Kiwa hirsuta. Environ. Microbiol. 10:2623–34 [Google Scholar]
  42. Goubern M, Andriamihaja M, Nubel T, Blachier F, Bouillaud F. 2007. Sulfide, the first inorganic substrate for human cells. FASEB J 21:1699–706 [Google Scholar]
  43. Greenway R, Arias-Rodriguez L, Diaz P, Tobler M. 2014. Patterns of macroinvertebrate and fish diversity in freshwater sulphide springs. Diversity 6:597–632 [Google Scholar]
  44. Grieshaber MK, Völkel S. 1998. Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu. Rev. Physiol. 60:33–53 [Google Scholar]
  45. Hand SC, Somero GN. 1983. Energy metabolism pathways of hydrothermal vent animals: adaptations to a food-rich and sulfide-rich deep-sea environment. Biol. Bull. 165:167–81 [Google Scholar]
  46. Hildebrandt TM, Grieshaber M. 2008. Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria. FEBS J 275:3352–61 [Google Scholar]
  47. Hochachka PW, Buck LT, Doll CJ, Land SC. 1996. Unifying theory of hypoxia tolerance: Molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. PNAS 93:9493–98 [Google Scholar]
  48. Holsinger JR. 2000. Ecological derivation, colonization, and speciation. Ecosystems of the World 30 Subterranean Ecosystems H Wilkens, DC Culver, WF Humphreys 399–415 Amsterdam: Elsevier [Google Scholar]
  49. Hourdez S, Weber RE, Green BN, Kenney JM, Fisher CR. 2002. Respiratory adaptations in a deep-sea orbiniid polychaete from Gulf of Mexico brine pool NR-1: metabolic rates and hemoglobin structure/function relationships. J. Exp. Biol. 205:1669–81 [Google Scholar]
  50. Huang J, Zhang L, Li J, Shi X, Zhang Z. 2013. Proposed function of alternative oxidase in mitochondrial sulphide oxidation detoxification in the Echiuran worm. Urechis unicinctus. J. Mar. Biol. Assoc. 93:2145–54 [Google Scholar]
  51. Ishigami M, Hiraki K, Umemura K, Ogasawara Y, Ishii K, Kimura H. 2009. A source of hydrogen sulfide and a mechanism of its release in the brain. Antioxid. Redox Signal. 11:205–14 [Google Scholar]
  52. Jackson MR, Melideo SL, Jorns M. 2012. Human sulfide:quinone oxireductase catalyzes the first step in hydrogen sulfide metabolism and produces a sulfane sulfur metabolite. Biochemistry 51:6804–15 [Google Scholar]
  53. Jahn A, Janas U, Theede H, Szaniawska A. 1997. Significance of body size in sulphide detoxification in the Baltic clam Macoma balthica (Bivalvia, Tellinidae) in the Gulf of Gdansk. Mar. Ecol. Prog. Ser. 154:1997 [Google Scholar]
  54. Jannasch HW, Taylor CD. 1984. Deep-sea microbiology. Annu. Rev. Microbiol. 38:487–514 [Google Scholar]
  55. Jones WJ, Won YJ, Maas PAY, Smith PJ, Lutz RA, Vrijenhoek RC. 2006. Evolution of habitat use by deep-sea mussels. Mar. Biol. 148:841–51 [Google Scholar]
  56. Jourdan J, Bierbach D, Riesch R, Schiessl A, Wigh A. et al. 2014. Microhabitat use, population densities, and size distributions of sulfur cave-dwelling Poecilia mexicana. PeerJ 2:e490 [Google Scholar]
  57. Julian D, Wieting SL, Seto SL, Bogan MR, Arp AJ. 1999. Thiosulfate elimination and permeability in a sulfide-adapted marine invertebrate. Physiol. Biochem. Zool. 72:416–25 [Google Scholar]
  58. Kelley JL, Arias-Rodriguez L, Patacsil Martin D, Yee M-C, Bustamante CD, Tobler M. 2016. Mechanisms underlying adaptation to life in hydrogen sulfide–rich environments. Mol. Biol. Evol. 33:1419–34 [Google Scholar]
  59. Kimura Y, Kimura H. 2004. Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18:1165–67 [Google Scholar]
  60. Kleiner M, Petersen JM, Dubilier N. 2012. Convergent and divergent evolution of metabolism in sulfur-oxidizing symbionts and the role of horizontal gene transfer. Curr. Opin. Microbiol. 15:621–31 [Google Scholar]
  61. Kojima S, Fujikura K, Okutani T. 2004. Multiple trans-Pacific migrations of the deep-sea vent/seep-endemic bivalves in the family Vesicomyidae. Mol. Phylogenet. Evol. 32:396–406 [Google Scholar]
  62. Kombian SB, Warenyica MW, Mele F, Reiffenstein RJ. 1988. Effects of acute intoxication with hydrogen sulfide on central amino acid transmitter systems. Neurotoxicology 9:587–96 [Google Scholar]
  63. Kump LR, Pavlov A, Arthur MA. 2005. Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia. Geology 33:397–400 [Google Scholar]
  64. Kyuno A, Shintaku M, Fujita Y, Matsumoto H, Utsumi M. et al. 2009. Dispersal and differentiation of deep-sea mussels of the genus Bathymodiolus (Mytilidae, Bathymodiolinae). J. Mar. Biol. 2009:625–72 [Google Scholar]
  65. Lagoutte E, Mimoun S, Andriamihaja M, Chaumontet C, Blachier F, Bouillaud F. 2010. Oxidation of hydrogen sulfide remains a priority in mammalian cells and causes reverse electron transfer in colonocytes. Biochim. Biophys. Acta 1797:1500–11 [Google Scholar]
  66. Laudien J, Schiedek D, Brey T, Pörtner H-O, Arntz WE. 2002. Survivorship of juvenile surf clams Donax serra (Bivalvia, Donacidae) exposed to severe hypoxia and hydrogen sulphide. J. Exp. Mar. Biol. Ecol. 271:9–23 [Google Scholar]
  67. Leffler CW, Parfenova H, Jaggar JH, Wang R. 2006. Carbon monoxide and hydrogen sulfide: gaseous messengers in cerebrovascular circulation. J. Appl. Physiol. 100:1065–76 [Google Scholar]
  68. Levesque C, Juniper S, Marcus J. 2003. Food resource partitioning and competition among alvinellid polychaetes of Juan de Fuca Ridge hydrothermal vents. Mar. Ecol. Prog. Ser. 246:173–82 [Google Scholar]
  69. Levin LA. 2005. Ecology of cold seep sediments: interactions of fauna with flow, chemistry, and microbes. Oceanogr. Mar. Biol. 43:1–46 [Google Scholar]
  70. Levin LA, Ziebis W, Mendoza G, Growney V, Tyron M. et al. 2003. Spatial heterogeneity of macrofauna at northern California methane seeps: the influence of sulfide concentration and fluid flow. Mar. Ecol. Prog. Ser. 265:123–39 [Google Scholar]
  71. Li L, Rose P, Moore PK. 2011. Hydrogen sulfide and cell signaling. Annu. Rev. Pharmacol. Toxicol. 51:169–87 [Google Scholar]
  72. Li Q, Lancaster JR Jr. 2013. Chemical foundations of hydrogen sulfide biology. Nitric Oxide 35:21–34 [Google Scholar]
  73. Liu X, Zhang L, Zhang Z, Ma X, Liu J. 2015. Transcriptional response to sulfide in the Echiuran worm Urechis unicinctus by digital gene expression analysis. BMC Genom 16:829 [Google Scholar]
  74. Lorion J, Kiel S, Faure B, Kawato M, Ho SYW. et al. 2013. Adaptive radiation of chemosymbiotic deep-sea mussels. Proc. R. Soc. B 280:20131243 [Google Scholar]
  75. Luther GW, Ma S, Trouborst R, Glazer B, Blickley M. et al. 2004. The roles of anoxia, H2S, and sorm events in fish kills of dead-end canals of Delaware inland bays. Estuaries 27:551–60 [Google Scholar]
  76. Ma Y-B, Zhang Z-F, Shao M-Y, Kang K-H, Shi X-L. et al. 2012. Response of sulfide-quinone oxireductase to sulfide exposure in the echiuran worm Urechis unicinctus. Mar. Biotechnol. 14:245–51 [Google Scholar]
  77. Marsh L, Copeley JT, Tyler PA, Thatje S. 2015. In hot and cold water, differential life history traits are key to success in contrasting thermal deep-sea environments. J. Anim. Ecol. 84:898–913 [Google Scholar]
  78. Martin NM, Maricle BR. 2015. Species-specific enzymatic tolerance of sulfide toxicity in plant roots. Plant Physiol. Biochem. 88:36–41 [Google Scholar]
  79. Martin W, Baross J, Kelley D, Russell MJ. 2008. Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6:805–14 [Google Scholar]
  80. Matabos M, Thiebaut E, Le Guen D, Sadosky F, Jollivet D, Bonhomme F. 2008. Geographic clines and stepping-stone patterns detected along the East Pacific Rise in the vetigastropod Lepetodrilus elevatus reflect species crypticism. Mar. Biol. 153:545–63 [Google Scholar]
  81. Mathai JC, Missner A, Kugler P, Saparov SM, Zeidel ML. et al. 2009. No facilitator required for membrane transport of hydrogen sulfide. PNAS 106:16633–38 [Google Scholar]
  82. McDonald AE, Vanlerberghe GC, Staples JF. 2009. Alternative oxidase in animals: unique characteristics and taxonomic distribution. J. Exp. Biol. 212:2627–34 [Google Scholar]
  83. McMullin E, Bergquist D, Fisher CR. 2000. Metazoans in extreme environments: adaptations of hydrothermal vent and hydrocarbon fauna. Gravit. Space Biol. J. 13:13–23 [Google Scholar]
  84. Micheli F, Peterson CH, Mullineaux LS, Fisher CR, Mills SW. et al. 2002. Predation structures communities at deep-sea hydrothermal vents. Ecol. Monogr. 72:365–82 [Google Scholar]
  85. Millero FJ. 1986. The thermodynamics and kinetics of the hydrogen sulfide system in natural waters. Mar. Chem. 18:121–47 [Google Scholar]
  86. Miron G, Kristensen E. 1993. Behavioral response of three nereid polychaetes to injection of sulfide inside burrows. Mar. Ecol. Prog. Ser. 101:147–55 [Google Scholar]
  87. Mullineaux LS, Fisher CR, Peterson CH, Schaeffer SW. 2000. Tubeworm succession at hydrothermal vents: use of biogenic cues to reduce habitat selection error. Oecologia 123:275–84 [Google Scholar]
  88. Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W. et al. 2009. H2S signals through protein S-sulfhydration. Sci. Signal. 2:ra72 [Google Scholar]
  89. Muyzer G, Stams AJM. 2008. The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 6:441–54 [Google Scholar]
  90. Nakagawa S, Tekai K. 2008. Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol. Ecol. 65:1–14 [Google Scholar]
  91. Newton ILG, Girguis PR, Cavanaugh CM. 2008. Comparative genomics of vesicomyd clam (Bivalvia: Mollusca) chemosynthetic symbionts. BMC Genom 9:585 [Google Scholar]
  92. Nosil P. 2012. Ecological Speciation Oxford, UK: Oxford Univ. Press [Google Scholar]
  93. Nussbaumer AD, Fisher CR, Bright M. 2006. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345–48 [Google Scholar]
  94. Oeschger R, Vetter RD. 1992. Sulfide detoxification and tolerance in Halicryptus spinulosus: a multiple strategy. Mar. Ecol. Prog. Ser. 86:167–79 [Google Scholar]
  95. Olson KR. 2011. The therapeutic potential of hydrogen sulfide: separating hype from hope. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301:R297–312 [Google Scholar]
  96. Olson KR, Straub KD. 2015. The role of hydrogen sulfide in evolution and the evolution of hydrogen sulfide in metabolism and signaling. Physiology 31:60–72 [Google Scholar]
  97. Peek AS, Feldmann R, Lutz R, Vrijenhoek RC. 1998. Conspeciation of chemoautotrophic bacteria and deep sea clams. PNAS 95:9962–66 [Google Scholar]
  98. Peers C, Bauer C, Boyle JP, Scragg JL, Dallas ML. 2012. Modulation of ion channels by hydrogen sulfide. Antioxid. Redox Signal. 17:95–105 [Google Scholar]
  99. Petersen JM, Wentrup C, Verna C, Knittel K, Dubilier N. 2012. Origins and evolutionary flexibility of chemosynthetic symbionts from deep-sea animals. Biol. Bull. 223:123–37 [Google Scholar]
  100. Pfenninger M, Lerp H, Tobler M, Passow CN, Kelley JL. et al. 2014. Parallel evolution of cox genes in H2S-tolerant fish as key adaptation to a toxic environment. Nat. Commun. 5:3873 [Google Scholar]
  101. Pfenninger M, Patel S, Arias-Rodriguez L, Feldmeyer B, Riesch R, Plath M. 2015. Unique evolutionary trajectories in repeated adaptation to hydrogen sulphide-toxic habitats of a neotropical fish (Poecilia mexicana). Mol. Ecol. 24:5446–59 [Google Scholar]
  102. Pietri R, Roman-Morales E, Lopez-Garriga J. 2011. Hydrogen sulfide and heme proteins: knowledge and mysteries. Antioxid. Redox Signal. 15:393–404 [Google Scholar]
  103. Plath M, Pfenninger M, Lerp H, Riesch R, Eschenbrenner C. et al. 2013. Genetic differentiation and selection against migrants in evolutionarily replicated extreme environments. Evolution 67:2647–61 [Google Scholar]
  104. Podowski EL, Ma S, Luther GW, Wardrop D, Fisher CR. 2010. Biotic and abiotic factors affecting distributions of megafauna in diffuse flow on andesite and basalt along the Eastern Lau Spreading Center, Tonga. Mar. Ecol. Prog. Ser. 418:25–45 [Google Scholar]
  105. Ponsard J, Cambon-Bonavita MA, Zbinden M, Lepoint G, Joassin A. et al. 2013. Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata. ISME J. 7:96–109 [Google Scholar]
  106. Powell E. 1989. Oxygen, sulfide and diffusion: why thiobiotic meiofauna must be sulfide-insensitive first-order respirers. J. Mar. Res. 47:887–932 [Google Scholar]
  107. Price A. 2002. Simultaneous ‘hotspots’ and ‘coldspots’ of marine biodiversity and implications for global conservation. Mar. Ecol. Prog. Ser. 241:23–27 [Google Scholar]
  108. Qu K, Lee SW, Bian JS, Low C-M, Wong PT-H. 2008. Hydrogen sulfide: neurochemistry and neurobiology. Neurochem. Int. 52:155–65 [Google Scholar]
  109. Riesch R, Oranth A, Dzienko J, Karau N, Schiessl A. et al. 2010. Extreme habitats are not refuges: Poeciliids suffer from increased aerial predation risk in sulphidic southern Mexican habitats. Biol. J. Linn. Soc. 101:417–26 [Google Scholar]
  110. Riesch R, Plath M, Schlupp I, Tobler M, Langerhans RB. 2014. Colonization of toxic springs drives predictable life-history shift in livebearing fishes (Poeciliidae). Ecol. Lett. 17:65–71 [Google Scholar]
  111. Riesch R, Tobler M, Garcia de Leon FJ, Schlupp I, Plath M. 2006. Reduction of the association preference for conspecifics in surface- and cave-dwelling Atlantic mollies. Poecilia mexicana. Behav. Ecol. Sociobiol. 60:794–802 [Google Scholar]
  112. Riesch R, Tobler M, Lerp H, Jourdan J, Doumas LT. et al. 2016. Extremophile Poeciliidae: multivariate insights into the complexity of speciation along replicated ecological gradients. BMC Evol. Biol. 16:136 [Google Scholar]
  113. Roach K, Tobler M, Winemiller KO. 2011. Hydrogen sulfide, bacteria, and fish: a unique, subterranean food chain. Ecology 92:2056–62 [Google Scholar]
  114. Roeselers G, Newton ILG. 2012. On the evolutionary ecology of symbioses between chemosynthetic bacteria and bivalves. Appl. Microbiol. Biotechnol. 94:1–10 [Google Scholar]
  115. Rosenzweig ML. 1978. Competitive speciation. Biol. J. Linn. Soc. 10:275–89 [Google Scholar]
  116. Salvanes AGV, Utne-Palm AC, Currie B, Braithwaite VA. 2011. Behavioral and physiological adaptations of the bearded goby, a key fish species of the extreme environment of the northern Benguela upwelling. Mar. Ecol. Prog. Ser. 425:193–202 [Google Scholar]
  117. Sancho G, Fisher CR, Mills S, Micheli F, Johnson GA. et al. 2005. Selective predation by the zoarcid fish Thermarces cerberus at hydrothermal vents. Deep-Sea Res. Part I 52:837–44 [Google Scholar]
  118. Sarbu SM, Kane TC, Kinkle BK. 1996. A chemoautotrophically based cave ecosystem. Science 272:1953–55 [Google Scholar]
  119. Shen X, Carlström M, Borniquel S, Jädert C, Kevil CG, Lundberg J. 2013. Microbial regulation of host hydrogen sulfide bioavailability and metabolism. Free Radic. Biol. Med. 60:195–200 [Google Scholar]
  120. Smith CR, Baco AR. 2003. Ecology of whale falls at the deep sea floor. Oceanogr. Mar. Biol. 41:311–54 [Google Scholar]
  121. Somero GN, Childress JJ, Anderson AE. 1989. Transport, metabolism, and detoxification of hydrogen sulfide in animals from sulfide-rich marine environments. Rev. Aquat. Sci. 1:591–614 [Google Scholar]
  122. Stipanuk MH, Ueki I. 2011. Dealing with methionine/homocysteine sulfur: cysteine metabolism to taurine and inorganic sulfur. J. Inherit. Metab. Dis. 34:17–32 [Google Scholar]
  123. Summers Engel A. 2007. Observations on the biodiversity of sulfidic karst habitats. J. Cave Karst Stud. 69:187–206 [Google Scholar]
  124. Szczesny B, Modis K, Yanagi K, Coletta C, Le Trionnaire S. et al. 2014. AP39, a novel mitochondria-targeted hydrogen sulfide donor, stimulates cellular bioenergetics, exerts cryoprotective effects and protects against the loss of mitochondrial DNA integrity in oxidatively stressed endothelial cells in vitro. Nitric Oxide 41:120–30 [Google Scholar]
  125. Teixeira S, Olu K, Decker C, Cunha RL, Fuchs S. et al. 2013. High connectivity across the fragmented chemosynthetic ecosystems of the deep Atlantic Equatorial Belt: efficient dispersal mechanisms or questionable endemism?. Mol. Ecol. 22:4663–80 [Google Scholar]
  126. Theissen U, Hoffmeister M, Grieshaber M, Martin W. 2003. Single eubacterial origin of eukaryotic sulfide:quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol. Biol. Evol. 20:1564–74 [Google Scholar]
  127. Theissen U, Martin W. 2008. Sulfide:quinone oxidoreductase (SQR) from the lugworm Arenicola marina shows cyanide- and thioredoxin-dependent activity. FEBS J 275:1–9 [Google Scholar]
  128. Thornhill DJ, Struck TH, Ebbe B, Lee RW, Mendoza GF. et al. 2012. Adaptive radiation in extremophilic Dorvilleidae (Annelida): diversification of a single colonizer or multiple independent lineages. Ecol. Evol. 2:1958–70 [Google Scholar]
  129. Thubaut J, Puillandre N, Faure B, Cruaud C, Samadi S. 2013. The contrasted evolutionary fates of deep-sea chemosynthetic mussels (Bivalvia, Bathymodiolinae). Ecol. Evol. 3:4748–66 [Google Scholar]
  130. Tiranti V, Viscomi C, Hildebrandt TM, Di Meo I, Mineri R. et al. 2009. Loss of the ETHE1, a mitochondrial dioxygenase, causes fatal sulfide toxicity in ethylmalonic encephalopathy. Nat. Med. 15:200–5 [Google Scholar]
  131. Tobler M, Palacios M, Chapman LJ, Mitrofanov I, Bierbach D. et al. 2011. Evolution in extreme environments: replicated phenotypic differentiation in livebearing fish inhabiting sulfidic springs. Evolution 65:2213–28 [Google Scholar]
  132. Tobler M, Plath M, Riesch R, Schlupp I, Grasse A. et al. 2014. Selection from parasites favors immunogenic diversity but not divergence among locally adapted host populations. J. Evol. Biol. 27:960–74 [Google Scholar]
  133. Tobler M, Riesch R, Tobler CM, Plath M. 2009. Compensatory behaviour in response to sulfide-induced hypoxia affects time budgets, feeding efficiency, and predation risk. Evol. Ecol. Res. 11:935–48 [Google Scholar]
  134. Tobler M, Scharnweber K, Greenway R, Passow CN, Arias-Rodriguez L, García-De-León FJ. 2015. Convergent changes in the trophic ecology of extremophile fish along replicated environmental gradients. Freshw. Biol. 60:768–80 [Google Scholar]
  135. Tobler M, Schlupp I, García de León FJ, Glaubrecht M, Plath M. 2007a. Extreme habitats as refuge from parasite infections? Evidence from an extremophile fish. Acta Oecol 31:270–75 [Google Scholar]
  136. Tobler M, Schlupp I, Plath M. 2007b. Predation of a cave fish (Poecilia mexicana, Poeciliidae) by a giant water-bug (Belostoma, Belostomatidae) in a Mexican sulfur cave. Ecol. Entomol 32:492–95 [Google Scholar]
  137. Tsurumi M. 2003. Diversity at hydrothermal vents. Glob. Ecol. Biogeogr. 12:181–90 [Google Scholar]
  138. Tunnicliffe V. 1991. The biology of hydrothermal vents: Ecology and evolution. Oceanogr. Mar. Biol. Annu. Rev. 29:319–407 [Google Scholar]
  139. Tunnicliffe V, Embley RW, Holden JF, Butterfield DA, Massoth GJ, Juniper S. 1997. Biological colonization of new hydrothermal vents following an eruption on Juan de Fuca Ridge. Deep-Sea Res. Part I 44:1627–44 [Google Scholar]
  140. Turnipseed M, Knick KE, Lipcius RN, Dreyer J, Van Dover CL. 2003. Diversity in mussel beds at deep-sea hydrothermal vents and cold seeps. Ecol. Lett. 6:518–23 [Google Scholar]
  141. Van Dover CL. 2000. The Ecology of Deep-Sea Hydrothermal Vents Princeton, NJ: Princeton Univ. Press [Google Scholar]
  142. Van Dover CL. 2007. Stable isotope studies in marine chemoautotrophically based ecosystems: an update. Stable Isotopes in Ecology and Environmental Science R Michener, K Lajtha, pp. 202–37 Malden, MA: Blackwell [Google Scholar]
  143. Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC. 2002. Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295:1253–57 [Google Scholar]
  144. Vanreusel A, De Groote A, Gollner S, Bright M. 2010. Ecology and biogeography of free-living nematodes associated with chemosynthetic environments in the deep sea: a review. PLOS ONE 5:e12449 [Google Scholar]
  145. Vismann B. 1991. Sulfide tolerance: physiological mechanisms and ecological implications. Ophelia 34:1–27 [Google Scholar]
  146. Völkel S, Grieshaber MK. 1997. Sulfide oxidation and oxidative phosphorylation in the mitochondria of the lugworm Arenicola marina. J. Exp. Biol. 200:83–92 [Google Scholar]
  147. Vrijenhoek RC. 2010. Genetic diversity and connectivity of deep-sea hydrothermal vent metapopulations. Mol. Ecol. 19:4391–411 [Google Scholar]
  148. Vrijenhoek RC. 2013. On the instability and evolutionary age of deep-sea chemosynthetic communities. Deep-Sea Res. Part II 92:189–200 [Google Scholar]
  149. Wang F, Chapman PM. 1999. Biological implications of sulfide in sediment: a review focusing on sediment toxicity. Environ. Toxicol. Chem. 18:2526–32 [Google Scholar]
  150. Ward ME, Shields JD, Van Dover CL. 2004. Parasitism in species of Bathymodiolus (Bivalva: Mytilidae) mussels from deep-sea seep and hydrothermal vents. Dis. Aquat. Organ. 62:1–16 [Google Scholar]
  151. Wohlgemuth SE, Taylor AC, Grieshaber M. 2000. Ventilatory and metabolic responses to hypoxia and sulphide in the lugworm Arenicola marina (L.). J. Exp. Biol. 203:3177–88 [Google Scholar]
  152. Xu Y, Schoonen MAA, Nordstrom DK, Cunningham KM, Ball JW. 1998. Sulfur geochemistry of hydrothermal waters in Yellowstone National Park: I. The origin of thiosulfate in hot spring water. Geochim. Cosmochim. Acta 62:3729–43 [Google Scholar]
  153. Zal F, Leize E, Lallier FH, Toulmond A, Van Dorsselaer A, Childress JJ. 1998. S-sulfohemoglobin and disulfide exchange: the mechanisms of sulfide binding by Riftia pachyptila hemoglobins. PNAS 95:8997–9002 [Google Scholar]
  154. Zhao W, Zhang J, Lu Y, Wang R. 2001. The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO J 20:6008–16 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error